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A Critical Role for the Right Fronto-Insular Cortex in Switching Between Central-Executive and Default-Mode Networks

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A Critical Role for the Right Fronto-Insular Cortex in Switching Between Central-Executive and Default-Mode Networks A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks Devarajan Sridharan*†‡, Daniel J. Levitin§, and Vinod Menon*†‡¶ *Department of Psychiatry and Behavioral Sciences, †Program in Neuroscience and ¶Neuroscience Institute at Stanford, Stanford University School of Medicine, Stanford, CA 94305 and §Department of Psychology, School of Computer Science and Program in Behavioural Neuroscience, McGill University, 1205 Avenue Penfield, Montreal, QC, Canada H3A 1B1 Edited by Marcus E. Raichle, Washington University School of Medicine, St. Louis, MO, and approved June 20, 2008 (received for review January 1, 2008) Cognitively demanding tasks that evoke activation in the brain’s In a recent meta-analysis, Dosenbach and colleagues hypoth- central-executive network (CEN) have been consistently shown to esized that several brain regions that overlap with the CEN and evoke decreased activation (deactivation) in the default-mode SN are important for multiple cognitive control functions, network (DMN). The neural mechanisms underlying this switch including initiation, maintenance, and adjustment of attention between activation and deactivation of large-scale brain networks (7). However, no studies to date have directly assessed the remain completely unknown. Here, we use functional magnetic temporal dynamics and causal interactions of specific nodes resonance imaging (fMRI) to investigate the mechanisms underly- within the CEN, SN, and DMN. Converging evidence from a ing switching of brain networks in three different experiments. We number of brain imaging studies across several task domains first examined this switching process in an auditory event seg- suggests that the FIC and ACC nodes of the SN, in particular, mentation task. We observed significant activation of the CEN and respond to the degree of subjective salience, whether cognitive, deactivation of the DMN, along with activation of a third network homeostatic, or emotional (4, 8–11). The CEN, on the other comprising the right fronto-insular cortex (rFIC) and anterior cin- hand, is critical for the active maintenance and manipulation of gulate cortex (ACC), when participants perceived salient auditory information in working memory, and for judgment and decision event boundaries. Using chronometric techniques and Granger making in the context of goal directed behavior (12–18). We NEUROSCIENCE causality analysis, we show that the rFIC-ACC network, and the therefore hypothesized a key role for the SN in the hierarchical rFIC, in particular, plays a critical and causal role in switching initiation of cognitive control signals, specifically with respect to between the CEN and the DMN. We replicated this causal connec- activation and deactivation in the CEN and DMN, and the tivity pattern in two additional experiments: (i) a visual attention dynamics of switching between these two networks. ‘‘oddball’’ task and (ii) a task-free resting state. These results We used three functional magnetic resonance imaging (fMRI) indicate that the rFIC is likely to play a major role in switching experiments to examine the interaction between the SN, CEN, between distinct brain networks across task paradigms and stim- and DMN, with particular interest in the role of the FIC/ACC in ulus modalities. Our findings have important implications for a regulating these networks. In the first experiment, we scanned 18 unified view of network mechanisms underlying both exogenous participants as they listened with focused attention to classical and endogenous cognitive control. music symphonies inside the scanner. We analyzed brain re- sponses during the occurrence of ‘‘movement transitions:’’ sa- brain networks ͉ cognitive control ͉ insula ͉ attention ͉ prefrontal cortex lient, orienting events arising from transitions between adjacent ‘‘movements’’ in the music (19). To specifically elucidate the role ne distinguishing feature of the human brain, compared of the FIC in driving network changes, we used chronometry and Owith brains lower on the phylogenetic ladder, is the amount Granger Causality Analysis (GCA), to provide information of cognitive control available for selecting, switching, and at- about the dynamics and directionality of signaling in cortical tending to salient events in the environment. Recent research circuits (20–22). suggests that the human brain is intrinsically organized into In the second experiment, we investigated the generality of distinct functional networks that support these processes (1–4). network switching mechanisms involving the FIC by examining Analysis of resting-state functional connectivity, using both brain responses elicited during a visual “oddball” attention task model-based and model-free approaches, has suggested the (23). A third experiment examined whether the network switch- existence of at least three canonical networks: (i) a central- ing mechanism could be observed during task-free resting state executive network (CEN), whose key nodes include the dorso- where there was no overt task and no behavioral response (4). lateral prefrontal cortex (DLPFC), and posterior parietal cortex Our motivation for examining the resting-state fMRI data was (PPC); (ii) the default-mode network (DMN), which includes the the recent finding, based on computer simulation of large-scale ventromedial prefrontal cortex (VMPFC) and posterior cingu- brain networks, that even in the absence of external stimuli, late cortex (PCC); and (iii) a salience network (SN), which certain nodes can regulate other nodes and function as hubs (24). includes the ventrolateral prefrontal cortex (VLPFC) and an- terior insula (jointly referred to as the fronto-insular cortex; FIC) Author contributions: V.M. designed research; D.S., D.J.L., and V.M. performed research; and the anterior cingulate cortex (ACC) (1, 2, 4, 5). During the D.S. analyzed data; and D.S. and V.M. wrote the paper. performance of cognitively demanding tasks, the CEN and SN The authors declare no conflict of interest. typically show increases in activation whereas the DMN shows decreases in activation (1, 2, 6). However, what remains un- This article is a PNAS Direct Submission. known is the crucial issue of how the operation of these ‡To whom correspondence may be addressed at: Program in Neuroscience and Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 780 Welch networks, identified in the resting state, relate to their function Road, Room 201, Stanford, CA 94305-5778. E-mail: [email protected] or menon@ during cognitive information processing. Furthermore, the cog- stanford.edu. nitive control mechanisms that mediate concurrent activation This article contains supporting information online at www.pnas.org/cgi/content/full/ and deactivation within these large-scale brain networks during 0800005105/DCSupplemental. task performance are poorly understood. © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0800005105 PNAS ͉ August 26, 2008 ͉ vol. 105 ͉ no. 34 ͉ 12569–12574 Downloaded by guest on October 1, 2021 Fig. 1. Activations in the Central-Executive and Salience Networks and deactivations in the Default-Mode Network during auditory event transitions. (A) Analysis with the General Linear Model (GLM) revealed regional activations (Left) in the right hemispheric FIC and ACC (blue circles); DLPFC and PPC (green circles) (coronal sections at y ϭϩ22, ϩ12 and Ϫ52 mm) and deactivations (Right) in the VMPFC and PCC (sagittal section at x ϭϩ4 mm and axial sections at z ϭϩ26 and Ϫ8 mm, yellow circles) during event transitions. The scale for t-scores is shown along side. Activations height and extent thresholded at the P Ͻ 0.01 level (corrected). (B) Independent Component Analysis (ICA, a model-free analysis technique) provided converging evidence for spatially independent and distinct networks. From left to right: Salience Network (rFIC and ACC), Central-Executive Network (rDLPFC and rPPC), and Default-Mode Network (VMPFC and PCC). Activations height and extent thresholded at the P Ͻ 0.001 level (uncorrected). The ICA prunes out extraneous activation and deactivation clusters visible in the GLM analysis to reveal brain regions that constitute independent and tightly coupled networks. Our aim was to test the hypothesis that common network this method provides a way to estimate the peak latency of the switching mechanisms apply across tasks with varying cognitive BOLD response at each voxel using the ratio of the derivative to demands and differing stimulus modalities. If confirmed, our canonical parameter estimates (see SI Materials and Methods for findings would provide insights into fundamental control mech- details). This analysis revealed that the event-related fMRI anisms in the human brain. signal in the right FIC (rFIC) and ACC peaks earlier compared to the signal in the nodes of the CEN and DMN, indicating that Results the neural responses in the rFIC and ACC precede the CEN and We describe findings from Experiment 1 in the first three DMN (see Fig. S1 and Table S2). To provide converging sections. Convergent findings from Experiments 2 and 3 are quantitative evidence, we estimated the onset latency of the described subsequently. blood oxygen level dependent (BOLD) response in these regions using the method of Sterzer and Kleinschmidt (27). Previous Activation of CEN and SN, and Deactivation of DMN During Auditory studies have used differences in the onset latency of the BOLD Event Segmentation.
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